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The Journal of Neuroscience, December 15, 2000, 20(24):9162-9173
Fine-Tuning an Auditory Synapse for Speed and Fidelity:
Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and
Synaptic Plasticity
Holger
Taschenberger and
Henrique
von Gersdorff
The Vollum Institute, Oregon Health Sciences University, Portland,
Oregon 97201
Fast, precise, and sustained synaptic transmission at high
frequency is thought to be crucial for the task of sound localization in the auditory brainstem. However, recordings from the calyx of Held
synapse have revealed severe frequency-dependent synaptic depression,
which tends to degrade the exact timing of postsynaptic spikes. Here we
investigate the functional changes occurring throughout the critical
period of synapse refinement from immature calyx terminal [postnatal
day 5 (P5)] to after the onset of hearing (P12-P14). Surprisingly,
for recordings near physiological temperature (35°C), we find that
P14 synapses are already able to follow extremely high input rates of
up to 800 Hz. This ability stems in part from a remarkable shortening
of presynaptic action potentials, which may lead to a lowering of
release probability and decrease in synaptic delays during development.
In addition, AMPA receptor-mediated EPSCs as well as quantal synaptic
currents acquired progressively faster kinetics, although their mean
amplitudes did not change significantly. NMDA receptor-mediated EPSCs,
however, diminished with age, as indicated by a 50% reduction in mean
amplitude and faster decay kinetics. Finally, the degree of synaptic
depression was greatly attenuated with age, presumably because of a
2.5-fold or larger increase in the releasable pool of vesicles, which
together with a decreasing release probability produces a fairly
constant EPSC amplitude. This finely tuned orchestra of developmental
changes thus simultaneously promotes speed while preventing premature vesicle pool depletion during prolonged bouts of firing. A few critical
days in postnatal development can thus have a large impact on synaptic function.
Key words:
development; MNTB; calyx of Held; AMPA and NMDA EPSCs; quantal and mEPSCs; short-term synaptic depression; patch-clamp; neuronal reliability
Copyright © 2000 Society for Neuroscience 0270-6474/00/20249162-12$05.00/0
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F. Mori-Kawakami, K. Kobayashi, and T. Takahashi
Developmental decrease in synaptic facilitation at the mouse hippocampal mossy fibre synapse
J. Physiol.,
November 15, 2003;
553(1):
37 - 48.
[Abstract]
[Full Text]
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T. Ishikawa, Y. Nakamura, N. Saitoh, W.-B. Li, S. Iwasaki, and T. Takahashi
Distinct Roles of Kv1 and Kv3 Potassium Channels at the Calyx of Held Presynaptic Terminal
J. Neurosci.,
November 12, 2003;
23(32):
10445 - 10453.
[Abstract]
[Full Text]
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L. Cathala, S. Brickley, S. Cull-Candy, and M. Farrant
Maturation of EPSCs and Intrinsic Membrane Properties Enhances Precision at a Cerebellar Synapse
J. Neurosci.,
July 9, 2003;
23(14):
6074 - 6085.
[Abstract]
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A. Y. C. Wong, B. P. Graham, B. Billups, and I. D. Forsythe
Distinguishing between Presynaptic and Postsynaptic Mechanisms of Short-Term Depression during Action Potential Trains
J. Neurosci.,
June 15, 2003;
23(12):
4868 - 4877.
[Abstract]
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T. Yamashita, T. Ishikawa, and T. Takahashi
Developmental Increase in Vesicular Glutamate Content Does Not Cause Saturation of AMPA Receptors at the Calyx of Held Synapse
J. Neurosci.,
May 1, 2003;
23(9):
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[Abstract]
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C. J Meinrenken, J G. G Borst, and B. Sakmann
Local routes revisited: the space and time dependence of the Ca2+ signal for phasic transmitter release at the rat calyx of Held
J. Physiol.,
March 15, 2003;
547(3):
665 - 689.
[Abstract]
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C. M. Macica, C. A. A. von Hehn, L.-Y. Wang, C.-S. Ho, S. Yokoyama, R. H. Joho, and L. K. Kaczmarek
Modulation of the Kv3.1b Potassium Channel Isoform Adjusts the Fidelity of the Firing Pattern of Auditory Neurons
J. Neurosci.,
February 15, 2003;
23(4):
1133 - 1141.
[Abstract]
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Y. Li and R. E. Burke
Developmental Changes in Short-Term Synaptic Depression in the Neonatal Mouse Spinal Cord
J Neurophysiol,
December 1, 2002;
88(6):
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[Abstract]
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P. D. Dodson, M. C. Barker, and I. D. Forsythe
Two Heteromeric Kv1 Potassium Channels Differentially Regulate Action Potential Firing
J. Neurosci.,
August 15, 2002;
22(16):
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[Abstract]
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J. Waters and S. J Smith
Vesicle pool partitioning influences presynaptic diversity and weighting in rat hippocampal synapses
J. Physiol.,
June 15, 2002;
541(3):
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[Abstract]
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O. Behrend, A. Brand, C. Kapfer, and B. Grothe
Auditory Response Properties in the Superior Paraolivary Nucleus of the Gerbil
J Neurophysiol,
June 1, 2002;
87(6):
2915 - 2928.
[Abstract]
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R. M. Leao and H. Von Gersdorff
Noradrenaline Increases High-Frequency Firing at the Calyx of Held Synapse During Development by Inhibiting Glutamate Release
J Neurophysiol,
May 1, 2002;
87(5):
2297 - 2306.
[Abstract]
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I. Joshi and L.-Y. Wang
Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem
J. Physiol.,
May 1, 2002;
540(3):
861 - 873.
[Abstract]
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T. Tsujimoto, A. Jeromin, N. Saitoh, J. C. Roder, and T. Takahashi
Neuronal Calcium Sensor 1 and Activity-Dependent Facilitation of P/Q-Type Calcium Currents at Presynaptic Nerve Terminals
Science,
March 22, 2002;
295(5563):
2276 - 2279.
[Abstract]
[Full Text]
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C. J. Meinrenken, J. G. G. Borst, and B. Sakmann
Calcium Secretion Coupling at Calyx of Held Governed by Nonuniform Channel-Vesicle Topography
J. Neurosci.,
March 1, 2002;
22(5):
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[Abstract]
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S. J Pyott and C. Rosenmund
The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons
J. Physiol.,
March 1, 2002;
539(2):
523 - 535.
[Abstract]
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V. Scheuss, R. Schneggenburger, and E. Neher
Separation of Presynaptic and Postsynaptic Contributions to Depression by Covariance Analysis of Successive EPSCs at the Calyx of Held Synapse
J. Neurosci.,
February 1, 2002;
22(3):
728 - 739.
[Abstract]
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C.-Y. Chen, E.-h. Ling, J. M Horowitz, and A. C Bonham
Synaptic transmission in nucleus tractus solitarius is depressed by Group II and III but not Group I presynaptic metabotropic glutamate receptors in rats
J. Physiol.,
February 1, 2002;
538(3):
773 - 786.
[Abstract]
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N. Chuhma and H. Ohmori
Role of Ca2+ in the Synchronization of Transmitter Release at Calyceal Synapses in the Auditory System of Rat
J Neurophysiol,
January 1, 2002;
87(1):
222 - 228.
[Abstract]
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H. Varoqui, M. K.-H. Schafer, H. Zhu, E. Weihe, and J. D. Erickson
Identification of the Differentiation-Associated Na+/PI Transporter as a Novel Vesicular Glutamate Transporter Expressed in a Distinct Set of Glutamatergic Synapses
J. Neurosci.,
January 1, 2002;
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[Abstract]
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S. Brenowitz and L. O. Trussell
Maturation of Synaptic Transmission at End-Bulb Synapses of the Cochlear Nucleus
J. Neurosci.,
December 1, 2001;
21(23):
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[Abstract]
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A. C. Meyer, E. Neher, and R. Schneggenburger
Estimation of Quantal Size and Number of Functional Active Zones at the Calyx of Held Synapse by Nonstationary EPSC Variance Analysis
J. Neurosci.,
October 15, 2001;
21(20):
7889 - 7900.
[Abstract]
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Y. Sahara and T. Takahashi
Quantal components of the excitatory postsynaptic currents at a rat central auditory synapse
J. Physiol.,
October 1, 2001;
536(1):
189 - 197.
[Abstract]
[Full Text]
[PDF]
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S. Iwasaki and T. Takahashi
Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem
J. Physiol.,
August 1, 2001;
534(3):
861 - 871.
[Abstract]
[Full Text]
[PDF]
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K. Futai, M. Okada, K. Matsuyama, and T. Takahashi
High-Fidelity Transmission Acquired via a Developmental Decrease in NMDA Receptor Expression at an Auditory Synapse
J. Neurosci.,
May 15, 2001;
21(10):
3342 - 3349.
[Abstract]
[Full Text]
[PDF]
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C.-Y. Chen, E.-h. Ling, J. M Horowitz, and A. C Bonham
Synaptic transmission in nucleus tractus solitarius is depressed by Group II and III but not Group I presynaptic metabotropic glutamate receptors in rats
J. Physiol.,
February 1, 2002;
538(3):
773 - 786.
[Abstract]
[Full Text]
[PDF]
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S. J Pyott and C. Rosenmund
The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons
J. Physiol.,
March 1, 2002;
539(2):
523 - 535.
[Abstract]
[Full Text]
[PDF]
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I. Joshi and L.-Y. Wang
Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem
J. Physiol.,
May 1, 2002;
540(3):
861 - 873.
[Abstract]
[Full Text]
[PDF]
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